PALAIOS, 2010, v. 25, p. 167–182 Research Article DOI: 10.2110/palo.2009.p09-054r

THE DECAPODA (CRUSTACEA) AS PREDATORS ON MOLLUSCA THROUGH GEOLOGIC TIME

CARRIE E. SCHWEITZER1* and RODNEY M. FELDMANN 2 1Department of Geology, Kent State University Stark Campus, 6000 Frank Ave. NW, North Canton, Ohio 44720, USA; 2Department of Geology, Kent State University, Kent, Ohio 44242, USA e-mail: [email protected]

ABSTRACT decapods and lineages known to have modern congeners that are durophagous. The relationship between predator and prey is a persistent theme in There are five major means by which decapods crush shells or eat marine paleontology. Herein we focus on the decapod Crustacea, the shelled prey that, as they require specialization of the appendages (see shrimps, lobsters, and crabs, and their role as predators on the Mollusca Lau, 1987 on extant forms), might be recorded in the body fossil record. through geologic time. Five major means by which decapods crush shells There are also several types of feeding that may only chip the shells or or eat shelled prey might be recorded in the body-fossil record, as they simply pry them open, which are often not apparent in the fossil record. require specialization of the appendages. These include use of (1) All types of feeding on shelled organisms must affect evolution of the heterochelous first pereiopods, (2) molariform teeth on the fingers of shelled organism, based on recent studies that illustrate how predation the chelae, (3) a curved proximal tooth on the movable finger of the chela, takes precedence over other aspects of the environment in driving (4) calcified mandibles, and (5) flattened pereiopods (walking legs). evolution (Stanley, 2008). Studies of predation, evolution, and Decapods have had adaptations for durophagous predation on mollusks escalation should, therefore, consider all decapods that have adapta- since the early Triassic. Durophagous adaptations had appeared among tions for durophagy or that have adaptations for durophagy in extant multiple clades by the Late Cretaceous. The myriad means by which forms, not just those that leave easily recognized marks on shells. decapods prey upon Mollusca, and the multiple uses for which pereiopods There are some a priori assumptions in all studies related to decapod and other appendages are adapted, suggests that predation studies should predation. One assumption is that the thickening of molluscan shells incorporate more decapod types and more types of predation when and the development of more ornate ornamentation on shells is an examining predation as a driver of evolution. evolutionary adaptation to survive increased durophagous predation (Vermeij, 1977a, 1987). A second assumption is that strong chelae INTRODUCTION armed with stout denticles evolved as a predatory device, rather than for any other function (Lee, 1995; Schenk and Wainwright, 2001). A One of the persistent themes in the literature on marine paleontology third assumption is that shell-crushing appendages or other parts were has been the effect of predation by decapod crustaceans on the used in a way similar to present-today representatives in the Decapoda. evolutionary biology of their prey—commonly, the Mollusca. This type Many adaptations facilitating capture and predation of Mollusca could of predation is called durophagy, defined as the consumption of prey also facilitate predation on such shelled prey as Bryozoa and with a hard shell or skeleton, most often by crushing or drilling Brachiopoda. (Aronson, 2001). Pelecypods and gastropods have evolved a variety of strategies to reduce the effects of decapod predation, including the Systematic Definitions evolution of thicker shells and various elements of ornamentation. This relationship has been considered part of the Mesozoic Marine Various groups of the Decapoda are defined in the following section. Revolution (MMR) (Vermeij, 1977a, 1987) and other evolutionary Definitions are arranged alphabetically for ease of use. events (Walker and Brett, 2002). Typically, the interpretation of the Anomura.—A diverse group in which the abdomen may be carried predator-prey relationship has been viewed heavily from the perspective behind or underneath the cephalothorax (body) or in a shell or other of the response of the prey species. Less attention has been placed on structure, such as sea anemones, and in which the last pair of the multiple strategies used by the predators, their concomitant pereiopods is generally reduced and the abdomen may be asymmetrical. morphological expression, and the fact that not all predation may be This group includes the king crabs, snow crabs, mole crabs, hermit obvious on shell remains in the fossil record. crabs, and squat lobsters. Nearly all decapods are categorized as generalists based on their Brachyura.—The true crabs, an apparently monophyletic lineage of dietary preference, although a few have an amazingly limited diet. decapod crustaceans holding a symmetrical abdomen entirely or mostly From the standpoint of the paleontological record, it is possible to infer under the cephalothorax and usually with five pairs of pereiopods, the the manner of food capture and manipulation based on the morphology first of which is chelate and the second through fifth are generally of the decapod. Thus, various styles of predation may be suggested even achelate, although some have chelate or pseudochelate fifth pereiopods. under circumstances in which little or no trace of predation is evident Crab.—A general term for a decapod crustacean with an abdomen on putative prey species. Approaching the predator-prey relationship that is held entirely or mostly under the cephalothorax. This group from this standpoint may reveal potential interactions that cannot be includes brachyurans and anomurans. deduced simply by studying effects on prey. Heterotrematous Crabs.—Brachyurans in which the females possess The purposes of this paper are to (1) review the major documented genital openings on the sternum (ventral surface) and the males possess adaptations for durophagy in the Decapoda and (2) document the first genital openings on the coxae of the fifth pereiopods. This group may appearance of adaptations known to facilitate durophagy in modern be monophyletic and is considered more derived than many other brachyurans; studies are ongoing (De Grave et al., 2009). Lobster.—A general term for a decapod crustacean in which the * Corresponding author. carapace and abdomen are well-calcified and the abdomen extends

Copyright G 2010, SEPM (Society for Sedimentary Geology) 0883-1351/10/0025-0167/$3.00 168 SCHWEITZER AND FELDMANN PALAIOS posteriorly from the cephalothorax. There are chelate (Astacidea, some Lobsters that have large, usually heterochelous, chelae are found Palinura), achelate (Palinura), and pseudochelate (Glypheoidea) chiefly in the superfamilies Nephropoidea and Enoplometopoidea lobsters. Extant achelate lobsters are commonly called spiny lobsters. within the Astacidea (see Supplementary Data1). The Nephropoidea Podotrematous Crabs.—Brachyurans in which both males and includes several extinct and extant lineages, and their claws tend to be females possess genital openings on the coxae of the pereiopods (fifth strongly heterochelous. Variation within the Nephropoidea is so great and third, respectively). The group is probably polyphyletic; studies are that it is difficult to generalize on the manner in which food is obtained ongoing (De Grave et al., 2009). This group is considered to embrace (Wassenberg and Hill, 1989). For example, a few taxa within the the most primitive brachyurans. Thaumastochelidae have extremely specialized claws, hypothesized to Thoracotrematous Crabs.—Brachyurans in which the both the males be adapted for raking the seafloor and grasping soft-bodied prey. Most and females possess genital openings on the sternum (ventral surface). nephropoids, however, have claws similar to those of the American The group may be monophyletic; studies are ongoing (De Grave et al., lobster. 2009). This group is considered to contain the most derived In the American lobster, Homarus americanus H. Milne Edwards, brachyurans. 1837, a member of the Nephropidae, the first pereiopods are heterochelous. These animals have a cylindrical carapace and carry Institutional Abbreviations the claws anterior to the carapace. We have observed that these animals typically move forward and backward rather than sideways so it is Listed below are the institutional abbreviations used in this paper. probable that they approach prey straight on. Prey is attacked by the BMNH: The Natural History Museum, London, UK. crusher claw and the majority of breakage accomplished by the UKKSU D: Decapoda Collection, Department of Geology, Kent chelipeds. Manipulation by the minor claw and mastication by the State University, Kent, Ohio, USA. mandibles would further comminute the shell material. Shells would be SDSMT: Museum of Geology, South Dakota School of Mines and shattered as a result, and we hypothesize that these fragments would be Technology, Rapid City, South Dakota, USA. indistinguishable from shell material that had been broken up by USNM: United States National Museum of Natural History, abiotic processes. Smithsonian Institution, Washington, D.C., USA. Oji et al. (2003), however, suggested that shells broken as a result of UT: University of Texas at Austin, Non-Vertebrate Paleontology durophagous predation might be recognizable. Studies of foregut Lab, Austin, Texas, USA. contents of Metanephrops spp. from Australia indicated a diet of fish, ZRC: Collections of Department of Zoology, National University of crustaceans, squid, and small amounts of pelecypods and gastropods Singapore. (Wassenberg and Hill, 1989). The forward-extended claws (Fig. 1C) were interpreted to be useful in attacking and grasping actively mobile prey. In another study, Thomas and Davidson (1962) noted poly- DECAPOD MORPHOLOGY AND MODES OF PREDATION chaetes, crustaceans, and pelecypods as food items in the diet of Nephrops norvegicus (Linnaeus, 1758), in the North Sea. Thus, Overview Nephropoidea clearly include Mollusca as part of their diet. Predation by decapods has often been considered as a driving force in In a study of the feeding habits of 15 species of hermit crabs in the the evolution of mollusks with strong shells (Vermeij, 1977a) and is Paguroidea, arrayed within the Paguridae, Pylochelidae, Diogenidae, facilitated by several morphological traits. Although primary emphasis and Parapaguridae, Schembri (1982) found that the often heterochelous has been placed on crushing by stout chelipeds, several other chelipeds may serve purposes of herbivory, scavenging, and closure of morphological adaptations, coupled with specialized predatory behav- the occupied shell rather than for predation. Predatory feeding was ior, are also used. If the relationship between the evolution and used in three species studied, all within the Paguroidae; one species each radiation of decapods is to be considered as a force in the MMR in the Paguridae, Parapaguridae, and Pylopaguridae used predatory (Vermeij, 1977a; Walker and Brett, 2002) and other evolutionary feeding as a secondary feeding habit after suspension feeding or events, it is necessary to evaluate all modes of predation that are scavenging. The only mollusks recorded as prey were small gastropods exhibited by the living representatives, some of which do not leave that were crushed by the major claw and ingested. evidence of predation on the prey species. Several morphological Heterochely in brachyurans (Figs. 1D–E) varies widely between taxa, adaptations can be easily observed in the fossil record, including genders, and age groups. The sum of morphological characters of heterochely, molariform teeth, a curved proximal tooth, and well- carapace shape, claw morphology, and claw orientation makes crabs calcified mandibles. Less likely to be observed in fossils are flattened remarkably versatile in their predatory habit. They are able to skillfully dactyls of pereiopods (walking legs) 2–5 or pereiopods 1–5 in achelate manipulate prey, using several different strategies for attacking hard- lobsters. shelled prey. The cheliped is typically carried transverse to the medial Heterochely.—Heterochely refers to the condition in which the chelae axis of the animal and tends to lie directly in front of the anterior of the first pereiopods, usually in lobsters and brachyurans, markedly margin. The motion of the pereiopods is quite broad as is the direction differ in size and often are used for different purposes. It is generally of movement of the animal, although the latter is typically sideways as used as a synonym for handedness, which refers to the condition in opposed to forward and backward. Complete crushing of the shell to which one claw is different from the other. A crusher claw (Figs. 1A–B) gain access to the soft tissue is often accomplished by a crusher claw. in a heterochelous pair is robust, stout, and often bears molariform Shearing is yet another highly specialized manner of breaking teeth interpreted to crush shells or other types of prey. A cutter claw mollusk shells. A pelecypod is positioned between the major claw and (Fig. 1B) is slender, longer, and bears smaller, sharper teeth interpreted the teeth along the anterolateral margin of the carapace, and the two to tear the tissue of prey into smaller pieces for mastication. Sometimes valves are opened by a shearing action (Lau, 1987). Williams (1978) heterochely does not involve a crusher and a cutter, but rather claws of observed shearing in the feeding habit of Scylla serrata (Forska˚l, differing shape or size. In these instances, the larger is called the major 1775). or master claw, and the smaller the minor claw. Heterochely is Molariform Teeth.—Molariform teeth are stout denticles along the considered to be an adaptation for predation (Herrick, 1909, p. 273; occlusal surface of the fingers of the chelae that aid in crushing Lau, 1987; Dietl and Vega, 2008) but can be an adaptation for other (Figs. 1A–B, D–E) (Herrick, 1909; Seed and Hughes, 1995; Dietl and uses, including mating rituals. Evidence of heterochely is commonly preserved in the fossil record. 1 www.paleo.ku.edu/palaios PALAIOS DECAPODA AS PREDATORS ON MOLLUSCA OVER GEOLOGIC TIME 169

FIGURE 1—A) Extremely large crushing claw of Homarus americanus (H. Milne Edwards, 1837), uncatalogued specimen in Kent State University collection. B) Homarus americanus, USNM 99746, showing left crushing claw and right cutting claw, dorsal view. C) Metanephrops binghami (Boone, 1927), USNM 170698, dorsal view. D–E) Callinectes sapidus Rathbun, 1896, KSU D 1079, dorsal view (D) and oblique frontal view (#) showing heterochelous crusher (right) and cutter (left) claws. F) Brachyuran fingers and molariform teeth, sieved from beach sediment at Calvert Cliffs, Maryland. G–H) Callinectes sapidus, thin section of a claw of an uncatalogued extant specimen modified from Waugh et al. (2006), showing wear pattern on denticle (arrows). Scale bars 1 cm, except where indicated.

Vega, 2008). These usually occur on the crusher or major chela in a teeth were worn away, indicating that they had been abraded heterochelous pair but can occur on claws that are not noticeably (Figs. 1G–H). The development of increased hardening and the heterochelous, such as in the brachyuran family Cancridae (Latreille, appearance of wear on the teeth is strong evidence that the animals 1802). They are often fortified with extra calcite, high-magnesium were engaged in durophagous predation. It may be possible to calcite, or phosphorus (Waugh et al., 2006). This feature is readily positively correlate such teeth with known durophagous predators in preserved in the fossil record; sieving molluscan fragments in Holocene modern oceans and to extend these correlations to fossils in which teeth sediments often yields only the hardened molariform portion of the are not necessarily large and molariform. Examination of teeth in claws, attesting to their resistance to wear both in life and in sediments geologically older specimens may make it possible to identify the onset (Fig. 1F). Thus, presence of these teeth is taken to indicate that the of durophagy and to document that the claws were serving this animal is adapted for durophagous predation, whether or not the claws purpose, in addition to any of their other functions. are heterochelous. Shell crushing can also be accomplished with claws Curved Proximal Tooth.—One of the best known methods of with denticles that are not molariform (Schenk and Wainwright, 2001). durophagous predation is that of tubercular peeling, in which There may be a test for the use of molariform teeth in durophagous gastropod shells are opened by crabs with very specialized chelipeds predation that has not been exploited to any extent. Waugh et al. (2006) (Shoup, 1968). The process involves chipping away the aperture in examined the microstructure of occlusal surfaces in Pleistocene and successive breaks to produce an arcuate reentrant around the aperture extant Callinectes sapidus Rathbun, 1896, and Scylla serrata Forska˚l, of the gastropod until the animal is released and extracted. The results 1775, and noted that the teeth and the claw tips were more dense, of this process are readily recognized in the fossil record, and an harder, and contained more phosphorous than the remainder of the extensive literature has resulted (Vermeij, 1987). The cheliped form fingers. Further, they noted that the cuticular laminations within the responsible for this manner of attack is exemplified by that of the 170 SCHWEITZER AND FELDMANN PALAIOS

FIGURE 2—A–B) Calappa lophos (Herbst, 1785), KSU D 335, dorsal view (B) and frontal view, showing modified tooth on right cheliped for chipping shell margins; scale bars 1 cm. C–D) Calappa sp., Eocene, digital images from Bittner (1875, pl. I, figs. 7a–b); arrows indicate curved proximal tooth on movable finger. brachyuran family Calappidae (Shoup, 1968) (Figs. 2A–B). The (Glaessner, 1969). With the exception of the abyssal genus, Polycheles propodus markedly broadens distally and the fixed finger tends to be Heller, 1862, all are extinct, and information about dietary habits is not relatively short. The dactylus bears a stout, protuberant denticle known. The chelae are extremely long, slender, and delicate, which oblique to the occlusal surface near its proximal end. When the tooth is suggests that they would be poorly adapted for crushing hard-shelled positioned so that the aperture lies between the tooth and the axis of the organisms (Fig. 3E). Their flattened shape suggests that they may have cheliped, the crab can rotate the claw slightly and nip off a piece of the ingested mollusks in a manner similar to the achelate palinuran forms margin (Lau, 1987). This process is continued until the prey is released. using their mandibles. The curved proximal tooth can be preserved in the fossil record, as long Lobsters within the Glypheoidea lack true chelae but have dactyli as the proximal portion of the movable finger is present (Figs. 2C–D). that extend either parallel or more or less at right angles to the axis of Mandibles.—The mandibles of decapods (Fig. 3), the first pair of the propodus; in the latter case, they occlude against the distal portion feeding appendages, can be well-calcified and used for durophagy of the propodus (Fig. 3F). Typically, they are only weakly hetero- (Figs. 3A–B). Mandibles are sometimes preserved in fossils, although chelous. The propodus in the Glypheidae typically bears a distal spine this region of the animal is often covered by such appendages as the that may permit the animals to grasp prey. The superfamily had an maxillipeds, so even if they are preserved, they are often not visible extensive geologic history, but extant forms are limited to two genera unless destructive techniques are used. The Infraorder Palinura, the from the Indo-Pacific (Forest, 2006). To our knowledge, their dietary spiny lobsters including the Palinuroidea and Eryonoidea, includes habits are not known. Glypheoids have an elongate, cylindrical various forms that may lack chelae but include mollusks as a regular carapace and carry the first pereiopod in front of the carapace in a part of their diet (Wassenberg and Hill, 1989; Robles et al., 1990). manner similar to the nephropids. Thus, they probably move forward Within the Palinuroidea, observations on the feeding habits of and backward, rather than sideways, approaching prey from the front. Panulirus interruptus (Randall, 1840) document manipulation of the If, indeed, they attack molluscan prey, we hypothesize that they prey using the pereiopods and chipping and breaking of shells using the probably manipulate the animals toward the mouth with the mandibles (Robles et al., 1990). The Palinuridae have a carapace that is pereiopods and crush the shell using the mandibles. All decapods have quadrate in transverse cross section; pereiopods of approximately mandibles, but because glypheids are typically preserved in lateral similar size that are carried in an anterolateral position; extremely aspect, the mandibles have not been exposed in fossils to our strong mandibles; and large, stout antennae that have a wide range of knowledge. motion (Figs. 3A–D). The animals generally move forward and Brachyurans, for example, the spider crab Notomithrax Griffin, 1963 backward, and they typically approach prey from the front. Studies (Woods, 1993), use the mandibles in chipping and biting, a process that on the foregut content of species of Linuparus White, 1847 confirm that involves nipping at the margin of a shell until access to the soft tissue is mollusks, both pelecypods and gastropods, form a substantial part of obtained. The result of the attack would be a shell damaged along part their diet (Wassenberg and Hill, 1989). of its margin. Another group of spiny lobsters, the Eryonoidea, have broad, Flattened Pereiopods.—Many decapods use flattened pereiopods flattened carapaces, and four to five pairs of chelate appendages other than the chelipeds to facilitate taking of shelled prey. Usually, the PALAIOS DECAPODA AS PREDATORS ON MOLLUSCA OVER GEOLOGIC TIME 171

FIGURE 3—A–B) Linuparus somniosus (Berry and George, 1972), ZRC 1999-0001, deposited in the Department of Zoology, National University of Singapore, ventral view (A), showing achelate pereiopods and large, strong mandibles, and dorsal view (B). C–D) Linuparus grimmeri (Stenzel, 1945), syntype UT 21067, ventral (C) and dorsal (D) surface. E) Polycheles typhos (Heller, 1862), KSU D311, dorsal view. F) Drawing of Glyphea regleyana (Desmarest, 1822; illustrated in E´ tallon,1859, pl. 3, fig. 11). G–H) Scyllarides nodifer (Stimpson, 1866), USNM 274950, dorsal view (H) and ventral view, showing flattened pereiopods and smaller, more delicate mandibles. Scale bars 1 cm. dactyl, the distalmost segment, is used. Dactyls are usually less well (Figs. 3G–H). The direction of motion of the animals may be forward, calcified than other segments of the decapod; articles of the walking legs backward, and sideways. Scyllarides squammosus (H. Milne Edwards, (pereiopods 2–5) are not as well preserved in fossils as the dorsal 1837) has been observed attacking mollusks by mounting a pelecypod, carapace or the chelipeds (pereiopod 1). grasping the commissure by some of the pereiopods, prying the shell The Scyllaridae, within the Palinura, bear a dorsoventrally com- open, and detaching the adductor muscles using another pereiopod, a pressed carapace; delicate mandibles; isochelous first pereiopods, process referred to as direct wedging by Lau (1987). The dactyls used in carried laterally or anterolaterally; and short, often foliaceous antennae this process are flattened, bladelike elements, not circular in cross 172 SCHWEITZER AND FELDMANN PALAIOS

FIGURE 4—A) Uncatalogued specimen of Lithophaga sp. showing bored and repaired region (arrow) in position of posterior adductor muscle. B) Enlargement of damaged region on same specimen (arrow). Scale bars 1 cm. section, as is more usual. Durophagous predation by scyllarids can be oval shape and beveled edge, as well as its position in the hinge of the very sophisticated. In some cases, the lobster simply grabs and pries the pelecypod shell. shells open, whereas in other cases, it may hover over the pelecypod Rochette et al. (2007), in addition to the techniques described by Lau until the animal opens the valve to resume respiration and feeding. At (1987), described predation on gastropods by winkling. This method that time, the lobster quickly inserts the dactyli into the open margin involves grasping the soft tissue of the snail. Using the major claw, the and attacks the muscles; this approach was referred to as patience crab rotates the soft body of the snail around the inner lip, while the attack by Lau (1987). Whichever approach is applied, the prey may minor claw rotates the shell in the opposite direction. The shell is left exhibit a slightly chipped margin or lack any evidence of attack. The undamaged; therefore, this method would go undetected in the fossil Scyllaridae must be considered significant predators, the role of which record. would not be recognized by simply examining prey species, because they Decapoda Known from Gut Content to Consume Mollusks.—Many range from the Early Cretaceous to the Holocene. types of decapods, not just those that crush, bore, or chip their prey, Brachyurans including spider crabs (Woods, 1993) apply pelecypod and undoubtedly more than are reported here, eat mollusks as a minor wedging and prying as techniques to enter the shell without necessarily component of their diet. Studies from which these data are taken damaging the shell itself or leaving evidence of the attack. Clam shells analyzed decapod gut contents; thus, it is not known how the animal can be wedged open as dactyls are inserted along the commissure, and took the prey. Many of the lineages have a lengthy fossil record; thus, the shell is forced open to an extent sufficient for another dactyl to be we infer that animals in these lineages would have exerted selective inserted into the shell to scrape loose the adductor muscles. pressure on Mollusca. The first appearance of each of the families is Alternatively, the dactyls can be inserted along the commissure and summarized in Supplementary Data1, so that the families can be the shell directly pried open. Thus, presence of spider crabs in the fossil considered in future studies of predation by Decapoda. record indicates that this type of predation pressure must have been The king crabs, Lithodidae, are generalized feeders and, not, to our present. knowledge, active predators. The stomach contents of Paralithodes Gastropods may be preyed upon by the predator grasping the animal brevipes (H. Milne Edwards and Lucas, 1841) yielded a broad variety of by soft tissue in order to prevent the operculum from closing. Using plant and animal material, the majority vegetal (Sasaki and Kuwahara, dactyls, the crab then removes some of the soft tissue until the animal 1999). Mollusk remains, limited to pelecypods, were incidental. can be released from the shell. Woods (1993) described Notomithrax Although king crabs bear large claws, they are apparently used for using its cheliped to block closure of the gastropod opening with the purposes other than durophagous predation. operculum and then grabbing the soft tissue to pull it out. No obvious Within the squat lobsters, Galatheoidea Samouelle, 1819, predatory evidence of this style of attack would result. behavior has been observed in Munida sarsi (Huus, 1935), but the Use of Unspecialized Chelae.—Often durophagy is accomplished observed prey were krill (Hudson and Wigham, 2003). Similarly, using unspecialized chelae. Chipping and peeling of the shell margin of examination of stomach contents of M. subrugosa (White, 1847) gastropods and pelecypods can be accomplished by predators that may indicated that mollusk remains comprised a minor part of the diet or may not have specialized crushing claws. In the event that the prey is (Romero et al., 2004). Galatheids apparently do not engage regularly in too robust or too large to crush, the predator may nip at the margin of durophagous predation on mollusks. In the Aeglidae, a freshwater the shell with the cheliped until access to the interior is achieved. This family within the Galatheoidea, examination of stomach contents type of attack is evident on the shell of the prey and may provide some indicated a small percentage of mollusk shell fragments, but the manner evidence of the relative size of the predator and prey (Lau, 1987; Seed, of food gathering was not noted (Santos et al., 2008). Aeglids possess 1993). stout chelipeds that might serve as shell crushing devices (Fig. 5). They A particularly sophisticated method of predation is that of boring, are mentioned here because this aquatic group had marine origins in the whereby the predator enters the shell by using the tip of the dactyl to Late Cretaceous (Feldmann, 1984). drill a hole into the hinge, expanding the hole by nipping around the The Anomura often bear large claws of various forms, many of margins of the hole, and separating the adductor muscle from the shell which could function as shell crushers, but none of the literature known (Figs. 4A–B). This process has been observed (Elner, 1978) as Carcinus to us documents durophagous predation on mollusks. Most seem to maenus (Linnaeus, 1758) bored into the mussel Mytilus edulis prefer plant material and probably are best characterized as herbivores (Linnaeus, 1758). Although this process is probably not widespread, and scavengers rather than aggressive predators. the scar should clearly indicate the style of predation. The scar is Within the Brachyura, members of the Plagusiidae eat mollusks as a distinguishable from gastropod drilling scars by its lack of a circular or minor component of their diet, although they are primarily algae eaters PALAIOS DECAPODA AS PREDATORS ON MOLLUSCA OVER GEOLOGIC TIME 173

as a minor part of its diet (Lovrich and Sainte-Marie, 1997; Squires and Dawe, 2003).

TIMING OF APPEARANCE OF DUROPHAGOUS SPECIALIZATIONS IN DECAPODA

Studies of predation and paleoecology have often included the Decapoda because they are known predators on various groups of animals in modern ecosystems. Thus, Decapoda were thought to be capable of driving evolution and escalation as far back as the mid- Paleozoic (Brett and Walker, 2002; Walker and Brett, 2002, p. 135), although major innovations for shell crushing generally were thought to appear, at least in the Brachyura, in the Cenozoic (Vermeij, 1977a, 2002; Walker and Brett, 2002). Recent work on the fossil record and the extant groups of Decapoda has greatly altered interpretations of the timing of appearance of the major lineages within the group and, thus, the timing of appearance of many of these major innovations (Table 1). Dietl and Vega (2008) reported that shell-crushing specializations in brachyuran crabs appeared during the Late Cretaceous. Specializations such as those seen in the Calappidae appeared as early as the Eocene, based upon breakage patterns of shells (Vermeij, 1987). This timing of FIGURE 5—Aegla sp., KSU D1077, dorsal view. Scale bar 1 cm. appearance of shell-crushing specializations in the Brachyura largely seems to be the case, although similar specializations had been present for some time in lobsters. (Samson et al., 2007). Species of Hepatus Latreille, 1802, of the family An important caveat in working with fossil decapod crustaceans is Aethridae, eat a broad diet that includes mollusks (Mantelatto and that their record can be extremely sparse. A species may be known from Petracco, 1997). Paromola Wood-Mason in Wood-Mason and Alcock, one or only a few specimens. For example, in Palaeopalaemon newberryi 1891, of the very long-ranging family Homolidae, eats small mollusks (Whitfield, 1880), the chela is known from one specimen. The data as a small but significant component of its diet (Mori, 1986; Cartes, presented in Supplementary Data1 represents the sum of all of the 1993). Individuals have been observed using their first pereiopods to known data on fossil decapod crustaceans, based upon a list of all extend into the bottom sediment, perhaps to grab buried prey (Cartes, known fossil decapod crustacean species (Schweitzer et al., 2010). We 1993). Geryon Krøyer, 1837, in the Geryonidae, generally inhabiting have examined type specimens, voucher specimens, or original deep-water environments in oceans today, eats mollusks as a small part literature for every record. of its diet (Cartes, 1993; Domingos et al., 2007). Members of the The confirmed fossil record for the Decapoda is extremely limited Superfamily Majoidea Samouelle, 1819, the spider crabs are most before the Triassic Period, despite the assumption that decapods with commonly reported as herbivores (Rorandelli et al., 2007), but some shell-crushing claws first occurred in the Devonian and radiated in the consume mollusks; this is hypothesized to be due largely to their small late Paleozoic (Brett and Walker, 2002). We consider the only and delicate chelipeds (Woods, 1993). Notomithrax, described earlier, confirmed mid-Paleozoic decapod, Palaeopalaemon Whitfield, 1880, applies wedging and chipping to ingest mollusks, and the snow crab from the Devonian of Ohio, Kentucky, and Iowa, to be a lobster with Chionoecetes Krøyer, 1838, is a benthic majid that eats clams and snails questionable affinities. Its appendages are poorly known; the propodus

TABLE 1—Major groups of decapods and timing of appearance of major adaptations to durophagy. Adaptation plotted during time interval of first confirmed appearance in fossil record. X 5 earliest record of group if different from earliest appearance of major adaptation; E 5 early; M 5 middle; L 5 late; H 5 Heterochelous first pereiopods; MT 5 molariform teeth on occlusal surface of fingers; CT 5 curved tooth on proximal end of movable finger; Ma 5 well-calcified, large mandibles. Numbers in parenthesis indicate number of families in which adaptation(s) appeared.

E. L. E. M. L. E. L. Taxon Paleozoic Triassic Triassic Jurassic Jurassic Jurassic Cretaceous Cretaceous Paleocene Eocene Post-Eocene

Chelate (clawed) lobsters X HMT Spiny lobsters X Ma (1) Hermit crabs (Anomura) X MT H Brachyura Podotrematous Crabs (most primitive crabs) Dakoticancroidea MT (1) Raninoidea MT (1) Heterotremata (derived crabs) Aethridae (includes modern H, MT, CT? Hepatus) Calappidae (includes Calappa) MT, CT Parthenopoidea H, MT (1) Cancridae MT Carpilioidea X H, MT (2) Xanthoidea sensu lato H, MT, CT (1) Xanthoidae sensu stricto H, MT (1) Eriphioidea H, MT (1) Goneplacoidea H, MT (1) Portunoidea (swimming crabs) H, MT (3) 174 SCHWEITZER AND FELDMANN PALAIOS of the first pereiopod looks rather like a mitten, and the dactylus is Major shell-crushing adaptations appeared in the Heterotremata, a unknown (Schram et al., 1978, text-fig. 4). Thus, it is not appropriate at group of more derived crabs, and the brachyuran lineage that embraces this time to consider this a decapod with a shell-crushing appendage, almost all shell-crushing crabs in modern oceans, during the due to insufficient evidence. Cretaceous, including the Calappoidea, Portunoidea, and Carpilioidea. Other Paleozoic and Triassic taxa originally referred to the Decapoda Interestingly, much of the literature on extant brachyurans with have been previously or are herein removed from the group. specializations for shell crushing is concentrated on these three Examination of the holotype (SDSNH 25139) of the Mississippian superfamilies or their close relatives. In addition to the Brachyura, Imocaris tuberculata Schram and Mapes, 1984, suggests that it is not a well-formed, large mandibles are known from palinurid lobsters of Late brachyuran decapod; it lacks key rostral, orbital, and dorsal carapace Cretaceous age (Woods, 1925–1931; Figs. 3C–D). features, such as a cardiac region, that are diagnostic of the group. It is The first documented appearance of an adaptation to the chelae or represented only by a carapace; no appendages or ventral surface are other part of the body for durophagy can occur after the first preserved. The recently described Imocaris colombiensis Racheboeuf occurrence of the family in the fossil record (Table 1). Fossil decapod and Villarroel, 2003, has no appendages preserved. The Permian crustaceans are, however, often preserved solely as dorsal carapaces; Palaeopemphix Gemmellaro, 1890, has been referred to the Phyllocar- this is especially true in carbonate rocks of the Jurassic, Eocene, and ida (Feldmann et al., 2004). The Triassic occurrence of the Eubrachyura Miocene (see, for example, Schweitzer and Feldmann, 2009; De Angeli (Rinehart et al., 2003) has already been reinterpreted as an arthropod of and Garassino, 2006; and Mu¨ller, 1984, respectively). Thus, claw unknown affinities (Schweitzer and Feldmann, 2005). Protoclytiopsis morphology for the first occurrence of the family may be unknown, as Birshtein, 1958, a member of the Erymidae, was confirmed as occurring it is for all those groups in our dataset in which the appearance of in latest Permian deposits (Schram, 1980), but no appendages were durophagous adaptations is later than the first occurrence. The actual preserved. It is the only other confirmed Paleozoic occurrence of appearance of durophagous adaptations could have been earlier; Decapoda. Thus, at this time, there is no reason to attribute a recovery of relevant appendages will be required to test this hypothesis. considerable, driving role for decapods in the escalation of molluscan After the Cretaceous, durophagous adaptations appeared within shell thickness, ornamentation, and other antipredator adaptations other groups of Brachyura. Confirmed first records of adaptations to before the Triassic. durophagy occurred in Paleocene occurrences of one superfamily, and Vermeij (2008) suggested that during the MMR, evolutionary several other families appeared within superfamilies that were already innovations mostly occurred during two periods, the Late Triassic to known to have adaptations to durophagy (see Supplementary Data1). Early Jurassic and the Late Cretaceous. Our examination of the The Eocene, like the Cretaceous, was a time of major radiation, as Decapoda suggests that innovations for durophagy were more broadly has long been known (Glaessner, 1969; Schram, 1986; Schweitzer, distributed in time and among groups (Table 1). We have identified the 2001b; Schweitzer et al., 2002; Fraaije, 2003; Feldmann, 2003; decapod infraorders, superfamilies, and families in which evolutionary Schweitzer and Feldmann, 2005). In the Eocene, several families first innovations for durophagy have evolved or in which durophagous occurred in the record, within superfamilies that have either behavior is well documented in extant forms, as well as the first known confirmed adaptations to shell-crushing in modern congeners appearance of those groups in the fossil record. We have also included (Fig. 6D) or reports of durophagy in modern congeners. Several extinct groups with known adaptations to durophagy or in which we families with durophagous adapatations made first appearances also, have inferred them based upon relationships and morphological the Calappidae, Carcinidae, Portunidae, and Xanthidae sensu stricto, similarity to extant forms. Table 1 contains summary data; see all of which had been preceded by appearances of other members of Supplementary Data1 for detailed data used throughout the following their respective superfamilies. discussion. During the Early Triassic, chelate lobsters exhibited heterochely. Synthesis Well-developed molariform teeth appeared in the early Jurassic. Anomuran hermit crabs exhibiting heterochely first occurred during The role of the Decapoda in the MMR and their pre- and post- the Late Jurassic. During the Late Triassic to Early Jurassic, spiny Mesozoic influence on molluscan prey must be considered in light of the lobsters appeared, which have congeners that are known to be timing of appearance of the various decapod lineages. Prior to the durophagous in modern oceans. Fossil spiny lobsters have the same Mesozoic, there is little record of Decapoda and virtually no record of general body form as extant Palinuridae and are inferred to have eaten their appendages (one confirmed genus and species). The primary shelled prey using mandibles as do extant forms. Recovery of fossils decapod predators during the Triassic and Jurassic would have been with preserved, robust mandibles would permit testing of this chelate lobsters and probably achelate lobsters that pried open shells or hypothesis. During the Middle Jurassic, confirmed members of the used their mandibles, based upon the fossil record of recognized Brachyura appeared, but no lineages with known specializations for adaptations to heterochely. In order to fully appreciate the role of durophagy. Shrimp taxa were abundant at this time as well, but did not decapods in the MMR, these types of predators must be considered and then, and do not now, have large chelae. Most do not exhibit chelae integrated into analyses of predatory behavior and relationships. It may adapted for durophagy, and extant shrimps generally do not exhibit be possible to determine if indeed shell priers do leave scars on mollusk durophagous behavior. shells, for example. A radiation of decapods with specializations for As noted by Vermeij (2008) for other lineages, the Late Cretaceous crushing shells is documented in the fossil record from the Early appears to have been a time of innovation within the Decapoda in Jurassic in lobsters and the Late Cretaceous in the Brachyura. Other terms of durophagous adaptations (Figs. 3C–D; 6A–C). Durophagous methods of molluscan predation were undoubtedly present prior to the characteristics are well known from Cretaceous brachyurans (Table 1). Cretaceous; those types leave less obvious scars, and they must be taken Notably, durophagous adaptations appeared in a broad range of taxa, into consideration as well. including lobsters and podotrematous and several superfamilies of It is also important to recognize that decapods have quite broad heterotrematous brachyurans. The appearance of durophagy in diets. Most will eat a broad variety of food items, with only a few numerous lineages suggests that although there may indeed by a groups that are very specialized. Many decapods considered to be phylogenetic component to durophagous adaptations, they also have mollusk specialists (e.g., see Vannini et al., 1989) will eat a wide variety arisen more than once. Clearly, the polyphyly of these adaptations is of food, including a small amount of mollusks. Claws may be used for shown in their appearance within the lobsters, anomurans, and multiple functions, some of which may be at odds with specializations brachyurans as well as in a variety of brachyuran lineages. for crushing prey. Non-claw-bearing decapods in fact eat mollusks now PALAIOS DECAPODA AS PREDATORS ON MOLLUSCA OVER GEOLOGIC TIME 175

FIGURE 6—A) Hoploparia stokesi (Weller, 1903), Late Cretaceous, Antarctica, showing well-developed heterochely. B) Longusorbis cuniculosus (Richards, 1975), Campanian, British Columbia, showing heterochely. C) Carcineretes woolacotti (Withers, 1922), holotype BMNH In. 20780, Late Cretaceous, Jamaica, showing heterochely. D) Harpactocarcinus sp., KSU D25, showing marked heterochely. Scale bars 1 cm. and undoubtedly did so in the past. Thus, all of these factors must be method of predation, the extent of predation, and the impact of the integrated into understanding the role of Decapoda in the MMR and predator on prey and vice versa. an understanding of predator-prey relationships through time. Heterochely CAVEATS TO ESCALATION STUDIES Heterochely undoubtedly is not an adaptation solely for predation; Examination of the biological literature on durophagy, chelipeds, thus, interpretation of a heterochelous fossil decapod taxon as a and diet preferences within the Decapoda indicates decapod chelae are durophagous predator could be erroneous or overly simplistic. remarkably plastic in their morphology and are used for multiple Possession of heterochelous appendages, while common and well activities (Seed and Hughes, 1995). Large pereiopods may not be used documented within certain decapod lineages, is more variable than is for eating, and other appendages may be used for durophagous feeding. generally acknowledged in the paleontological literature. Smith and Bilateral asymmetry seems to be widespread among active, mobile Palmer (1994) demonstrated that claw size can change under artificial organisms (Babcock, 1993, 2005); thus, the observation that probably circumstances. If a crab is forced to use one claw over another, that all decapods are heterochelous to some extent, even though the claw will become stronger to compensate for the loss of use of the other difference in claws may only be a few millimeters in one or more claw; this also happens in nature. If a claw of a brachyuran is lost due to dimensions (Vermeij, 1977b). Heterochely serves a variety of functions autotomy, the crab will reverse handedness following the next molt other than food gathering, including display, defense, mate selection, cycle (Simonson, 1985). Thus, heterochely is advantageous but is also and clasping during reproduction (Lee, 1995; Schenk and Wainwright, plastic and can change with relative ease, the selective advantages of 2001). Many morphological features and behavioral habits other than which are manifold. crusher claws and strong heterochely provide evidence of predatory There is an extensive literature documenting reversal of handedness behavior, and further, other selective pressures have been at work in crabs and the age and molt number at which it occurs (Hamilton et besides escalation to produce a larger and stronger claw. Studies of al., 1976; Simonson, 1985, and references therein). If the crab was predation must account for a full suite of features to determine the initially right handed, it will become left handed after molting, thus 176 SCHWEITZER AND FELDMANN PALAIOS eliminating any advantage that may have been served by handedness. crushing arose numerous times and in numerous lineages in decapod Although handedness is initially fixed in many brachyurans, they are history (Jurassic–Paleogene) (Table 1), based on the fossil record. able to survive if handedness changes, as switching handedness after Plasticity is undoubtedly a large part of what makes crustaceans, and autotomy demonstrates. Thus, the evolutionary advantage of being arthropods in general, so successful. Plasticity is also what makes it right handed and the ability to subdue dextrally coiled snails, for difficult to assign a direct cause-and-effect relationship to the example (Ng and Tan, 1984), can be lost during growth and molting. development of specialized appendages in crustaceans. The decapod Other selective pressures besides those driving preference for handed- appendage is used for many functions and has demonstrated ness must be at work. considerable plasticity within the lifetime of one individual, not to Also interesting is that many crabs regrow claws after autotomy and mention over generations. The many selection pressures on the decapod will often exhibit two cutter claws instead of a crusher and a cutter appendage and the entire morphology of the decapod must be claw. Two ideas have been advanced for this response; one is that once considered, therefore, when integrating it into predator-prey studies. the cutter is regrown, it is relatively easy for it to change into a crusher Claws are multiuse appendages, and the uses for predation must be claw (Przibram, 1931), and the other is that possessing two cutter claws balanced by uses for scavenging, mating, display, and defense (Lee, must be more advantageous than having two crusher claws (Hamilton 1995). Marked heterochely in decapods is sometimes used for sexual et al., 1976). Having two cutter claws is not disadvantageous because display (Labadie and Palmer, 1996; Go´es and Fransozo, 1997), and the crabs survive, which has interesting implications for shell-crushing heterochely may have originated for this purpose, not for feeding. predation. Crabs can survive without the adaptation and, thus, must be Males generally have larger claws than females and exhibit more broadly adapted to eating a varied diet. Handedness and heterochely marked dimorphism in the chelae than do females. Some degree of are beneficial to the shell-crushing decapod but are not factors critical sexual selection has operated on appendages within the Decapoda, and to their survival. this is likely to be balanced with selection pressures for predation Handedness in decapods apparently can have a genetic basis within advantage in these same appendages. some lineages but may not in others. Herrick (1909) noted that the Some studies have indicated that males seem to ingest larger number of right handed (handedness is defined as bearing the crusher quantities of mollusks than do females, based upon the larger size of on the right side) and left handed individuals of the American lobster, the chelipeds in males of some species (e.g., Sukumaran and Homarus americanus, was about equal (differing by about 100 in a Neelakantan, 1997). Larger, heavier male claws appear to be better sample of over 2000 individuals). He concluded as had others before able to crush hard-shelled prey, permitting feeding on stronger, more him that lobsters do not appear to exhibit a strong preference for robust prey and reducing intraspecific competition. This results in handedness. Some brachyurans, on the other hand, seem to be strongly partitioning of resources so that males and females do not compete for right handed. Numerous studies have indicated that brachyurans, at the same food items. The study by Hamilton (1976) demonstrated a least among certain superfamilies, begin life right handed (Przibram, similar partitioning of resources. Primarily immature females or small 1931; Abby-Kalio and Warner, 1989), although this can change later as adult male blue crabs (Callinectes sapidus Rathbun, 1896) preyed upon the crab either molts or loses its first pereiopod due to autotomy. snails of the genus Littorina Ferussac, 1822, apparently due to their A genetic component of handedness is suggested by several other small size. Larger crabs of either sex are presumed to have preferred factors. Muscles in crushers and cutters are different. Crushers often larger prey and were able to crush it with their generally larger and have slower, stronger muscle fibers and cutters have faster muscles more dimorphic claws, resulting in resource partitioning. In the (Warner and Jones, 1976; Warner, 1977). The muscle types are Cancridae, numerous studies indicate that larger crabs are more reconfigured when claws are removed to accommodate the reversal of successful at crushing shells, perhaps due to the overall larger size of handedness (Govind and Pearce, 1994), indicating some level of genetic their claws (Creswell and Marsden, 1990). Thus, smaller crabs must control over the process. Exposure of alpheid shrimps to ecdysal resort to other means by which to obtain meals, and specialized chelae hormones can similarly accelerate molting and the reorganization of may only be advantageous once a certain size is reached. muscle tissue in response to reversal of handedness, thus indicating at Niche partitioning of resources may have been a secondary benefit of least some molecular control over the process (Mellon and Greer, sexual selection resulting in sexual dimorphism and development of 1987). There must also be some inherent nerve differences that sexual display in males. The more markedly dimorphic, larger claws in accompany handedness and switching from right to left, as claws are males permit or force them to eat different prey. Such patterns are even used for different purposes (Hamilton et al., 1976). noted in such crabs with isochelous claws as the cancrids and some Evolution from the reptant form to the brachyuran form may have xanthids (Figs. 7A–B), in which males or larger crabs simply have facilitated the selection for handedness, which could explain why the larger claws overall. Biological literature is apparently somewhat split lobsters do not display it and crabs do. Such an event as mutation may on the issue of niche partitioning as a result of sexual selection in have facilitated handedness occurred later in the brachyuran lineage, Decapoda (Lee, 1995, and references therein), but this issue seems to be possibly more than once, as the crusher and cutter phenomena are seen a fruitful avenue of research. in the heterotrematous crabs, and only in certain superfamilies Predation studies should also investigate chelae that are not (Calappoidea, Carpilioidea, Xanthoidea, Eriphioidea, Portunoidea). heterochelous and not overemphasize heterochelous claws. Members Interestingly, members of the genus Uca Leach, 1814, a thoracotrema- of the Cancridae Latreille, 1802, have been well documented as tous crab, do not exhibit preferred handedness (Abby-Kalio and durophagous, and they exhibit heterochely only on the order of a few Warner, 1989). The podotrematous crabs do not exhibit strong millimeters between the two chelae (Vermeij, 1977b). Thus, heterochely tendencies for handedness either. Thus, investigations of possible is not a prerequisite for durophagy, which suggests that many more decapod predation in which handedness seems to be a dominant feature groups in the fossil record may have been durophagous and currently might focus on the heterotreme lineages. are not recognized as such. Plasticity in handedness, the ability to switch the crusher from right An example of problems for feeding arising from extreme heterochely to left or for one claw to grow stronger if the other is lost, was suggested can be found in Pseudocarcinus gigas Lamarck, 1818, a huge crab that by Smith and Palmer (1994) to be a possible origin of heterochely in may weigh up to 14 kg (Heeren and Mitchell, 1997) and that has the evolutionary history. A simple need, or the simple advantage, of being largest chelipeds among the decapods (Hale, 1927; Heeren and able to break a molluscan shell could very rapidly result in specialized, Mitchell, 1997). These crabs possess robust, dimorphic claws with heterochelous first pereiopods. Thus, it should not be surprising that crushing molariform teeth that do not really fit into the categories of heterochely and other specializations in pereiopod morphology for shell crusher and cutter (Heeren and Mitchell, 1997, fig. 1). Heeren and PALAIOS DECAPODA AS PREDATORS ON MOLLUSCA OVER GEOLOGIC TIME 177

FIGURE 7—A–B) Atergatis floridus (Linnaeus, 1767), KSU D341, dorsal view (A) and frontal view , showing nearly equal sized crushing chelipeds. C) Palaeonephrops browni (Whitfield, 1907), KSU D1113, Late Cretaceous of Montana, showing extremely large claw for the species; note that the fingers would not occlude. Scale bars 1 cm.

Mitchell (1997) reported that males had a difficult time using their since at least the Jurassic. In what ways have many of these thin-shelled enormous, usually right, claw to manipulate food, using mainly the left mollusks responded? Are they simply not eaten often enough to claw, whereas females were able to manipulate food much more easily respond by developing thick shells or spines? Have they responded by as they do not exhibit such marked dimorphism. In this case, it seems going deeper in overall water depth? Do they dig deeper into the that the marked dimorphism hinders food gathering, and may instead sediment than they once did? Are they smaller and faster (i.e., harder to be an adaptation to mating display (Heeren and Mitchell, 1997; Taylor, catch)? Are they larger and, therefore, harder to manage? Has their 2001). Thus, it is important to keep such multiple uses of chelipeds in survival strategy emphasized fecundity over strength of individuals? mind when evaluating the fossil record. Interpretation of some fossil These are questions that need to be addressed and, in fact, can be, taxa with huge, markedly heterochelous claws as efficient shell-crushers because we do know the fossil record of the decapod families exhibiting may be erroneous (Megaxantho Vega et al., 2001; Tumidocarcinus such dietary preferences. Glaessner, 1960; some species of Harpactocarcinus A. Milne-Edwards, 1862; and some species of Trichopeltarion A. Milne-Edwards, 1880). Multiple Feeding Strategies Marked gape between fingers or the relationship between carapace width and claw size may suggest that the claw is used more for sexual Most decapods which possess claws that are considered to be display and less for shell crushing, despite marked heterochely specialized for crushing hard-shelled prey, in fact, consume a broad and (Fig. 7C). varied diet (Vannini et al., 1989; Mori et al., 1995). Vannini et al. (1989) reported that some species of Eriphia Latreille, 1817, do very little Durophagy without Robust Claws crushing to obtain nutrition when living in a rocky, intertidal environment. In addition, they noted that those species that did ingest Many studies of predator-prey relationships focus on shell ornamen- snail shells seemed to do so especially when hermit crabs inhabited tation, thickness, spines, and other easily measured criteria in prey, those shells. This suggests a much more complex relationship between because they are readily observed. Predators would drive escalation predator, prey, and the intermediate form—the gastropod that toward these features which make it more difficult to break shells. produced the shell that is used by the hermit crab—than is usually Numerous studies have demonstrated this trend (Vermeij, 1977a). A considered in paleontological studies. Monodaeus couchii (Couch, clawed organism, no matter how weak the claw, however, can break at 1851), a member of the Xanthidae sensu stricto, is a known predator least a thin shell (Dietl and Vega, 2008). Decapods have been of mollusks, but it actually feeds on a wide variety of organisms and is documented to possess claws since at least the Triassic, and probably also a deposit feeder and a scavenger (Mori et al., 1995). Even those as early as the Devonian, so they may have been breaking shells as at decapods exhibiting durophagous specializations are broadly adapted least an incidental part of their diet since that time. A broad range of to a variety of feeding strategies, perhaps in part as a response to extant decapods ingest at least small numbers of pelecypods and evolutionary processes within the Mollusca. Carcinus Leach, 1814 can gastropods, mostly thin shelled, as part of their diet, probably eating crush shells with molariform teeth, but also uses the winkling process them whole or crushing them with their mandibles or other mouthparts. described earlier (Rochette et al., 2007). Thus, the specialized crushing This must have exerted selection pressure on the Mollusca, as teeth are not always used to catch and crush prey. Cartes (1993) representatives of many of these extant decapods have been present described both Paromola Wood-Mason in Wood-Mason and Alcock, 178 SCHWEITZER AND FELDMANN PALAIOS

1891, and Geryon Krøyer, 1837, as opportunists, taking advantage of documented to engage in all styles of durophagous food gathering must be available prey and scavenging depending on the season. considered at the level of family or superfamily in order to obtain reliable Generalizations about the use of first pereiopods are very difficult to results in the determination of the role of decapods in driving the evolution make because the Decapoda are so varied and the first pereiopod is so of prey species in the MMR and at other times. plastic and multifunctional. Predators often evolve multiple mecha- nisms to subdue prey, an example of classic escalation. A crushing chela ACKNOWLEDGMENTS is useful but not the only means by which to subdue molluscan prey. As gastropods and pelecypods adapted to survive crushing specializations, NSF grant EF-0531670 to Feldmann and Schweitzer funded travel to decapods similarly evolved other mechanisms to subdue prey, some of the United States National Museum of Natural History, Smithsonian which leave few to no traces on the shells of prey. This type of Institution, Washington, D.C.; the South Dakota School of Mines and escalation is, thus, difficult to directly measure but can be inferred by Technology Museum of Geology, Rapid City; and the University of the presence in the fossil record of members of the same families that Texas, Austin, as well as travel to museums in Europe and South exhibit such behavior today. Escalation must be balanced by selective America and field work in Maryland. This work permitted accumula- pressures operating on these same appendages for other functions. tion of much of the fossil data presented herein. NSF grants INT- Thus, decapods must have reasonably broad adaptations to permit 0313606 and INT-0003058 to Feldmann and Schweitzer and NSF grant them to eat a broad variety of prey. The broad range of behaviors and OPP-9909184 to Feldmann and K. L. Bice funded field work, which preferences within the Decapoda must be accounted for in predation formed the basis for some of the fossil data presented here. R. Lemaitre, studies, and perhaps, signs of predation other than direct shell damage K. Reed, and J. Thompson generously facilitated our visits to the might be sought. USNM. A. Molineaux, University of Texas, Austin, loaned specimens of Linuparus. C. Melish accommodated our visit to the Natural History SUMMARY AND CONCLUSIONS Museum, London, UK. S. Shelton kindly permitted our extensive access to the G. A. Bishop Collection at the South Dakota School of Paleontological literature has primarily focused on three adaptations Mines and Technology Museum of Geology. S. H. Tan, National of decapods to durophagous predation on mollusks: heterochely, University of Singapore facilitated the loan of Linuparus somniosus.D. molariform teeth, and a curved tooth for shell peeling, because they Waugh, A. Hull, and C. Robins, all of KSU, assisted with collection of have a high preservation potential in the fossil record. Other such Holocene specimens of molariform teeth in Maryland, and O. Tshudy, adaptative morphologies as stout mandibles and flattened dactyls of the Edinboro, Pennsylvania, helped sort them from the sediment. R. L. M. walking legs are occasionally preserved. Examination of shape of the Ross, British Columbia, Canada, donated the specimen of Longusorbis cephalothorax, such as the transversely flattened shape typical of cuniculosis to KSU. Constructive comments were made on an earlier mandible crushers, is also important and may bear on timing of draft of the manuscript by G. Dietl, Paleontological Research appearance and style of predation preserved in the fossil record. Access Institution, Ithaca, and A. Klompmaker, Kent State University. S. to the soft tissue of molluscan prey can be achieved by numerous Walker, Department of Geology, University of Georgia, and three methods involving the chelipeds, the dactyli of the pereiopods, the anonymous reviewers provided helpful comments on the manuscript. mandibles, or some combination of these parts. Examination of the fossil record of decapod crustaceans with preserved evidence of these REFERENCES adaptations, or inferred presence of these adaptations due to morphological similarity to or relationship with extant taxa, shows ABBY-KALIO, N. J., and WARNER, G. F., 1989, Heterochely and handedness in the that durophagous adaptations arose in the Mesozoic, and especially in shore crab Carcinus maenas (L.) (Crustacea: Brachyura): Zoological Journal of the the Late Cretaceous, in most major groups. Linnean Society, v. 96, p. 19–26. Many taxa within the decapod crustaceans, particularly the lobsters ARONSON, R. B., 2001, Durophagy in marine organisms, in Briggs, D.E.G., and and true crabs, use subtle durophagous predation as a significant part Crowther, P.R., eds., Palaeobiology II: Backwell Science, Oxford, p. 393–397. BABCOCK, L. E., 1993, The right and the sinister: Natural History, v. 102, p. 32–39. of their feeding behavior. Animals so adapted are distributed among BABCOCK, L., 2005, Asymmetry in the fossil record: European Review, v. 13, several different superfamilies, and each taxon possesses a unique set of Supplement No. 2, p. 135–143. morphological features that facilitate predation. It appears that there is BELL, T., 1850, Notes on the Crustacea of the Chalk Formation, in Dixon, F., ed., The some genetic control on the morphology of predation that is expressed Geology and Fossils of the Tertiary and Cretaceous Formations of Sussex:Brown, at the level of superfamily or family. Green, and Longmans, London, p. 344–345, pl. 38. Emphasis on heterochely and development of very large, crusher BELL, T., 1858, A monograph of the fossil malacostracous Crustacea of Great Britain, claws as predatory tools might imply that the appendages coevolved as Pt. I: Crustacea of the London Clay: Monograph of the Palaeontographical Society, London, v. 10 [1856], p. i–viii, 1–44, 11 pl. their shelled prey became larger, stouter, and more ornamented. BELL, T., 1863, A monograph of the fossil malacostracous Crustacea of Great Britain, Recognition that the major claw serves a multitude of functions other Pt. II: Crustacea of the Gault and Greensand: Monograph of the Palaeonto- than predation, however, suggests that it is just as likely that one of graphical Society, London, p. 1–40, 11 pl. these other functions was the selective force for its development. BERRY, P.F., and GEORGE, R.W., 1972, A new species of the genus Linuparus Indeed, in at least one case, the major claw has grown so large that it (Crustacea, Palinuridae) from South-East Africa: Zoologische Mededelingen cannot function as a predatory device. (Leiden), v. 46, p. 17–23, pl. 1–2. Although numerous groups within the reptant Decapoda have been BEURLEN, K., 1930, Vergleichende Stammesgeschichte Grundlagen, Methoden, Probleme unter besonderer Beru¨cksichtigung der ho¨heren Krebse: Fortschrifte in documented to be durophagous predators, others prey upon soft-bodied der Geologie und Pala¨ontologie, v. 8, p. 317–586. organisms, and some ingest shelled organisms as incidental parts of their BIRSHTEIN, Y.A., 1958, Drevneishii predstavitel otryada desyatinogikh rakoobraz- diet probably while grazing, scavenging, or sifting sediment. In order to nykh Protoclytiopsis antiqua gen. nov. sp. nov. is permskikh otlozhenii zapadnoi carefully assess the role of decapods as predators through time, therefore, Sibiri: Comptes rendus de l’Academie des Sciences de l’URSS, v. 122, p. 477–480. it is important to view the process from the standpoint of the predator as BISHOP, G.A.,1988, Two crabs, Xandaros sternbergi (Rathbun 1926) n. gen., and well as the prey. This must involve examination of food resources Icriocarcinus xestos n. gen., n. sp., from the late Cretaceous of San Diego County, California, USA, and Baja California Norte, Mexico: Transactions of the San exploited by taxa; recognition that the possession of heterochelous, large Diego Society of Natural History, v. 21, p. 245–257. claws may have nothing to do with durophagous predation; and BISHOP, G.A., FELDMANN, R. M., and VEGA, F. J., 1998, The Dakoticancridae observation that animals superficially lacking in predatory tools may, in (Decapoda, Brachyura) from the Late Cretaceous of North America and Mexico: fact, be active predators. The geologic range of the taxa that have been Contributions to Zoology, v. 67, p. 237–255. PALAIOS DECAPODA AS PREDATORS ON MOLLUSCA OVER GEOLOGIC TIME 179

BITTNER, A., 1875, Die Brachyuren des vicentinischen Tertia¨rgebirges: Denkschriften FELDMANN, R.M., GARASSINO, A., and SCHWEITZER, C.E., 2004, The presumed der kaiserlichen Akademie der Wissenschaften Mathematisch-Naturwissenschaf- decapod, Palaeopemphix Gemmellaro, 1890, is a unique member of the tliche Klasse, v. 34, p. 63–105, pl. 1–5. Phyllocarida (Palaeopemphicida: Palaeopemphidae): Journal of Paleontology, v. BOONE, L., 1927, Crustacea from tropical east American seas: Scientific results of the 78, p. 340–348. first oceanographic expedition of the Pawnee, 1925: Bulletin of the Bingham FELDMANN, R.M., TSHUDY, D.M., and THOMSON, M.R.A., 1993, Late Cretaceous and Oceanographic Collection, v. 1, p. 1–147. Paleocene decapod crustaceans from James Ross Basin, Antarctic Peninsula: The BRETT, C.E., and WALKER, S.E., 2002, Predators and predation in Paleozoic marine Paleontological Society Memoir, 28, p. i–iv, 1–41. environments, in Kowalewski, M., and Kelley, P.H., eds., The Fossil Record of FELDMANN, R.M., SCHWEITZER, C.E., REDMAN, C.M., MORRIS, N.J., and WARD, D.J., Predation: The Paleontological Society Papers, v. 8: The Paleontological Society, p. 2007, New Cretaceous lobsters from the Kyzylkum Desert of Uzbekistan: Journal 93c¸118. of Paleontology, v. 81, p. 701–713. BROOKS, H.K., 1962, The Paleozoic Eumalacostraca of North America: Bulletins of FERUSSAC, A.E.J. D’AUDEBARD DE, 1821–1822, Tableaux syste´matiques des animaux American Paleontology, v. 44, p. 221–338. mollusques suivis d’un Prodrome ge´ne´ral pour tous les mollusques terrestres ou BUSULINI, A., TESSIER, G., and VISENTIN, M., 1984, Titanocarcinus aculeatus nuova fluviatiles vivants ou fossiles: Premie`re partie, Tableaux syste´matiques ge´ne´raux, p. specie di Brachiuro dell’Eocene del Veneto (Crustacea, Decapoda): Lavori— i–xlvii. Deuxie`me partie, Tableaux particuliers des mollusques terrestres et Societa` Veneziana di Scienze Naturali, v. 9, p. 107–117. fluviatiles, Classe des Gaste´ropodes: 1, Tableau de la famille des limaces, p. 1– CARTES, J. E., 1993, Diets of deep-sea brachyuran crabs in the Western Mediterranean 28; 2, Tableau de la famille des limac¸ons, p. 1–92. 3, Tableau de la famille des Sea: Marine Biology, v. 117, p. 449–457. auricules, p. 93–114: Arthus-Bertrand, Paris. COLOSI, G., 1923, Una specie fossile de Gerionide (Decapodi brachiuri): Bolettino FOREST, J., 2006, Laurentaeglyphea, un nouveau genre pur la second espe`ce actuelle de della Societa´ dei Naturalisti in Napoli, 35 (series 2, vol. 15), 37, p. 248–255. Glyphe´ide re´cemment de´couvert (Crustacea Decapoda Glypheidae): Comptes COUCH, R. Q., 1851, Notice of a Crustacea new to Cornwall: Transactions of the Rendus Biologies, v. 329, p. 841–846. Natural History and Antiquities Society of Penzance, v. 2, p. 13–14. FORSKA˚ L, P., 1775, Descriptiones animalium, avium, amphibiorum, piscium, CRESWELL, P. D., and MARSDEN, I. D., 1990, Morphology of the feeding apparatus of insectorum, vermium; quae in itinere orientali observavit Petrus Forska˚l: Mo¨lleri, Cancer novaezelandiae in relation to diet and predatory behaviour: Pacific Science, Hauniae (5Copenhagen), 164 p. v. 44, p. 384–400. FO¨ RSTER, R., 1966, Uber die Erymiden, eine alte konservative Familie der DANA, J.D., 1851a, On the classification of the Cancroidea: American Journal of mesozoischen Dekapoden: Palaeontographica, v. 125, p. 61–175. Science and Arts, Series 2, v. 12, p. 121–131. FRAAIJE, R.B., 2003, Evolution of reef-associated decapod crustaceans through time, DANA, J.D., 1851b, Paguridae: Conspectus Crustaceorum quae in Orbis Terrarum with particular reference to the Maastrichtian type area: Contributions to Zoology, circumnavigatione, Carolo Wilkes e Classe Reipublicae Foederatae Duce, lexit et v. 72, p. 119–130. descripsit: Proceedings of the Academy of Natural Sciences of Philadelphia, v. 5, p. GARASSINO, A., TERUZZI, G., and DALLA VECCHIA, F., 1996, The macruran decapod 267–272. crustaceans of the Dolomia di Forni (Norian, Upper Triassic) of Carnia (Udine, DANA, J.D., 1852, Crustacea, in U.S. Exploring Expedition During the Years 1838, NE Italy): Atti della Societa` Italiana di Scienze Naturale e del Museo Civico di 1839, 1840, 1841, 1842, under the Command of Charles Wilkes, U.S.N., Volume Storia naturale di Milano, v. 136, p. 15–60. 13: C. Sherman, Philadelphia, p. 390–400. GEMMELLARO, G.G., 1890, I crostacei dei calcari con Fusulina della Valle del Fiume DE ANGELI, A., and GARASSINO, A., 2006, Catalog and bibliography of the fossil Sosio nella Provincia di Palermo in Sicilia: Memorie della Societa` Italiana delle Stomatopoda and Decapoda from Italy: Memorie della Societa` Italiana di Scienze Scienze, v. 8, p.1–40, pl. 1–5. Naturali e del Museo Civico di Storia Naturale in Milano, v. 35: p. 1–95. GLAESSNER, M.F., 1931, Eine Crustaceenfauna aus den Lunzer Schichten Nieder- DE GRAVE, S., PENTCHEFF, N.D., AHYONG, S.T., CHAN, T.-Y., CRANDALL, K.A., o¨sterreichs: Jahrbuch der k. k. Geologischen Bundesanstalt Wien, v. 81, p. 467– DWORSCHAK, P.C., FELDER, D.L., FELDMANN, R.M., FRANSEN, C.H.J.M., GOULD- 486, pl. 15–16. ING, L.Y.D., LEMAITRE, R., LOW, M.L., MARTIN, J.W., NG, P.K.L., SCHWEITZER, GLAESSNER, M.F., 1960, The fossil decapod Crustacea of New Zealand and the C.E., TAN S.H., TSHUDY, D., and WETZER, R., 2009, A classification of Recent and evolution of the Order Decapoda: New Zealand Geological Survey Paleontological fossil genera of decapod Crustaceans: The Raffles Bulletin of Zoology Supplement Bulletin, v. 31, p. 1–79. 21, p. 1–109. GLAESSNER, M.F., 1969, Decapoda, in Moore, R.C., ed., Treatise on Invertebrate DESMAREST, A.G., 1822, Histoire Naturelle des Crustace´s Fossiles. Les Crustace´s Paleontology, Part R4(2):Geological Society of America, Boulder, Colorado, and Proprement Dits: F. G. Levrault, Paris, p. 67–154, pl. V–XI. University of Kansas Press, Lawrence, Kansas, p. R400–R533, R626–R628. DIETL, G., and VEGA, F.J., 2008, Specialized shell-breaking crab claws in Cretaceous GO´ ES J.M. DE, and FRANSOZO, A., 1997, Heterochely in Eriphia gonagra (Fabricius, seas: Biology Letters, v. 4, p. 290–293. 1781) (Crustacea, Decapoda, Xanthidae) of the rocky coast from Praia Grande, DOMINGOS, S.S., ATHIE, A.A.R., and ROSSI-WONGTSCHOWSKI, C.L.B., 2007, Diet of Ubatuba (SP), Brazil: Biotemas, v. 11, p. 71–80. Chaceon notialis (Decapoda, Brachyura) off the coast of Rio Grande, RS, Brazil: GOVIND, C.K., and PEARCE, J., 1994, Muscle remodeling in adult snapping shrimps via Brazilian Journal of Oceanography, v. 55, p. 327–329. fast-fiber degeneration and slow-fiber genesis and transformation: Cell Tissue ELNER, R. W., 1978, The mechanics of predation by the shore crab, Carcinus maenas Research, v. 276, p. 445–454. (L., on the edible mussel, Mytilus edulis L.: Oecologia (Berlin), v. 36, p. 333–344. GRIFFIN, D.J.G., 1963, Notomithrax gen. nov. and the status of the genus Paramithrax E´ TALLON, M. A., 1859, Description des crustace´s fossiles de la Haute-Sao´ne it du H. Milne Edwards (Crustacea, Brachyura, Majidae): Transactions of the Royal Haut-Jura: Bulletin de la Socie´te´Ge´ologique de France, Deuxieme se´rie, v. 16, p. Society of New Zealand, Zoology, v. 3, p. 229–237. 169–205, pl. 3–6. HAAN W. DE, 1833–1850, Crustacea, in Von Siebold, P F., ed., Fauna Japonica sive E´ TALLON, M. A., 1861, Notes sur les Crustace´s Jurassiques du bassin du Jura: Descriptio Animalium, quae in Itinere per Japoniam, Jussu et Auspiciis Super- Me´moires de la Societe´ de l’Agriculture, des Sciences et Lettres de la Haute Saoˆne, iorum, qui summum in India Batava Imperium Tenent, Suscepto, Annis 1823–1830 v. 9, p. 129–171, pl. 2. Collegit, Notis, Observationibus et Adumbrationibus Illustravit: Lugduni-Bata- FELDMANN, R. M., 1984, Haumuriaegla glaessneri n. gen. and sp. (Decapoda; vorum (5 Leiden): J. Mu¨ller et Co., i–xvii, i–xxxi, ix–xvi, p. 1–243, pl. A–J, L–Q, Anomura; Aeglidae) from Haumurian (Late Cretaceous) rocks near Cheviot, New 1–55, circ. Tab. 2. Zealand: New Zealand Journal of Geology and Geophysics, v. 27, p. 379–385. HALE, H.M., 1927, The Crustaceans of South Australia. Part 1: Adelaide, South FELDMANN, R. M., 1989, Metanephrops jenkinsi n. sp. (Decapoda: Nephropidae) from Australia Government Printer, 201 p. the Cretaceous and Paleocene of Seymour Island, Antarctica: Journal of HAMILTON, P.V., 1976, Predation on Littorina irrorata (Mollusca: Gastropoda) by Paleontology, v. 63, p. 64–69. Callinectes sapidus (Crustacea: Portunidae): Bulletin of Marine Science, v. 26, p. FELDMANN, R.M., 1998, Paralomis debodeorum, a new species of decapod crustacean 403–409. from the Miocene of New Zealand: First notice of the Lithodidae in the fossil HAMILTON, P.V., NISHIMOTO, R.T., and HALUSKY, G.J., 1976, Cheliped laterality in record: New Zealand Journal of Geology and Geophysics, v. 41, p. 35–38. Callinectes sapidus (Rathbun): Biological Bulletin of the Marine Biological FELDMANN, R.M., 2003, The Decapoda: New initiatives and novel approaches: Laboratory, Woods Hole, v. 150, p. 393–401. Journal of Paleontology, v. 77, p. 1021–1039. HEEREN, T., and MITCHELL, B.D., 1997, Morphology of the mouthparts, gastric mill FELDMANN, R.M., and SCHWEITZER, C.E., 2009, Revision of Jurassic Homoloidea de and digestive tract of the giant crab, Pseudocarcinus gigas (Milne Edwards) Haan, 1839, from the Ernstbrunn and Sˇtramberk limestones, Austria and the (Decapoda: Oziidae): Marine and Freshwater Research, v. 48, p. 7–18. Czech Republic: Annalen des Naturhistorischen Museums in Wien, Serie A, v. 111, HELLER, C., 1862, Neue Crustaceen, gesammelt wa¨hrend der Weltumseglung der k. k. p. 183–206. Fragatte Novara: Zweiter vorla¨ufiger Vericht: Verhandlungen der kaiserlischko¨- FELDMANN, R.M., and WILSON, M.T., 1988, Eocene decapod crustaceans from niglichen zoologisch-botanischen Gesellschaft in Wien, v. 12, p. 519–528. Antarctica, in Feldmann, R.M., and Woodburne, M.O., eds., Geology and HERBST, J.F.W., 1782–1804, Versuch einer Naturgeschichte der Krabben und Krebse Paleontology of Seymour Island, Antarctic Peninsula: Geological Societyof nebst einer systematischen Beschreibung ihrer verschiedenen Arten, volume 1 America Memoir 169, p. 465–488. (1782–1790), p. 1–274, pl. 1–21; volume 2 (1791–1796), p. i–viii, iii, iv, 1–225, pl. 180 SCHWEITZER AND FELDMANN PALAIOS

22–46; volume 3 (1799–1804), p. 1–66, pl. 47–50: G. A Lange, Berlin; J. C. Fuessly, MACLEAY, W.S., 1838, On the Brachyurous Decapod Crustacea brought from the Zu¨rich. Cape by Dr. Smith, in Smith, A., Illustrations of the Annulosa of South HERRICK, F.H., 1909, Natural history of the American lobster: Bulletin of the Bureau Africa, consisting chiefly of Figures and Descriptions of the Objects of Natural of Fisheries, v. 29, p. 149–408, pl. 33–47. History Collected during an Expedition into the Interior of South Africa, in the HUDSON, I.R., and WIGHAM, B.D., 2003, In situ observations of predatory feeding Years 1834, 1835, and 1836; fitted out by ‘‘The Cape of Good Hope behaviour of the galatheid squat lobster Munida sarsi using a remotely operated Association for Exploring Central Africa: Smith, Elder and Company, London, vehicle: Journal of the Marine Biological Association of the United Kingdom, v. p. 53–71, 2 pl. 83, p. 463–464. MANTELATTO, F.L.M., and PETRACCO, M., 1997, Natural diet of the crab Hepatus HUGHES, R.N., 1989, Foraging behaviour of a tropical crab: Ozius verreauxii: pudibundus (Brachyura: Calappidae) in Fortaleza Bay, Ubatuba (SP), Brazil: Proceedings of the Royal Society of London (B), v. 237, p. 201–212. Journal of Crustacean Biology, v. 17, p. 440–446. HUUS, J., 1935, Zur morphologisch-systematischen und biologischen Kenntnis der MELLON,JR., D., and GREER, E., 1987, Induction of precocious molting and claw nordischen Munida-Larven (Crustacea Decapoda), Bergens Museum Aarbok, v. 8 transformation in alpheid shrimps by exogenous 20-hydroxyecdysone: Biological (1934), p. 1–29, fig. 1–6, pl. 1–4. Bulletin, v. 172, p. 350–356. JENKINS, R. J. F., 1972, Metanephrops, a new genus of late Pliocene to Recent lobsters MCCOY, F., 1849, On the classification of some British fossil Crustacea with notices of (Decapoda, Nephropidae): Crustaceana, v. 22, p. 161–177. new forms in the university collection at Cambridge: Annals and Magazine of KARASAWA, H., 1992, The crab, Ozius collinsi sp. nov. (Crustacea: Decapoda: Natural History (2) v. 4, p. 161–179, 330–335. Xanthoidea) from the Miocene Katsuta Group, southwest Japan: Tertiary MCLAY, C.L., FELDMANN, R.M., and MACKINNON, D.I., 1995, New species of Research, v. 14, p. 19–24. Miocene spider crabs from New Zealand, and a partial cladistic analysis of the genus Leptomithrax Miers, 1876 (Brachyura: Majidae): New Zealand Journal of KARASAWA, H., and KATO, H., 1996, Daldorfia Rathbun, 1904 (Crustacea, Decapoda) from the Neogene of Japan: Proceedings of the Biological Society of Washington, Geology and Geophysics, v. 38, p. 299–313. v. 109, p. 44–52. MILKE, L.M., and KENNEDY, V.S., 2001, Mud crabs (Xanthidae) in Chesapeake Bay: claw characteristics and predation on epifaunal bivalves: Invertebrate Biology, v. KARASAWA, H., and KATO, H., 2003, The family Goneplacidae MacLeay, 1838 (Crustacea: Decapoda: Brachyura): Systematics, phylogeny, and fossil records: 120, p. 67–77. Paleontological Research, v. 7(2), p. 129–151. MILNE-EDWARDS, A.,1862, Monographie des crustace´s fossiles de la famille des canceriens: Annales de Science Naturelle, Zoologie, Series 4, v. 18, p. 31–85, pl. 1– KARASAWA, H., and SCHWEITZER, C.E., 2006, A new classification of the Xanthoidea sensu lato (Crustacea: Decapoda: Brachyura) based on phylogenetic analysis and 10. ` e`re traditional systematics and evaluation of all fossil Xanthoidea sensu lato: MILNE-EDWARDS, A., 1880, Etudes pre`liminaires sur les Crustace´s, 1 Partie: Reports Contributions to Zoology, v. 75(1/2), p. 23–73. on the Results of Dredging under the Supervision of Alexander Agassiz, in the Gulf of Mexico, and in the Caribbean Sea, 1877, ’78, ’79, by the U.S. Coast Guard KARASAWA, H., SCHWEITZER, C.E., and FELDMANN, R.M., 2008, Revision of the Survey Steamer ‘Blake,’ Lieutenant-Commander C. D. Sigsbee, U. S. N., and Portunoidea Rafinesque, 1815 (Decapoda: Brachyura) with emphasis on the fossil Commander J. R. Bartlett, U. S. N., commanding, VIII: Bulletin of the Museumof genera and families: Journal of Crustacean Biology, v. 28, p. 82–127. Comparative Zoology, Harvard, v. 8, p. 1–68, pl. 1–2. KESLING, R.V., and REIMANN, I.G., 1957, An Upper Cretaceous crab, Avitelmessus MILNE EDWARDS, H., 1834–1840, Histoire naturelle des Crustace´s, comprenant grapsoideus Rathbun: Contributions to the Museum of Paleontology, University of l’anatomie, la physiologie, et la classification de ces animaux: Vol. 1, 1834, 468 p.; Michigan, v. 14, p. 1–15. Vol. 2, 1837, 532 p.; Vol. 3, 1840, 638 p.; atlas, 32 p., pl. 1–42. KRØYER, H., 1837, Geryon tridens, en ny Krabbe: Naturhistorisk Tidsskrift, v. 1, p. MILNE EDWARDS, H., 1853, Me´moires sur la famille des Ocypodiens, suite: Annales du 10–21, pl. 1. Science Naturelles, Zoologie (3), v. 20, p. 163–228, pl. 6–11. KRØYER, H., 1838, Conspectus Crustaceorum Groenlandiae: Naturhistorisk Tids- MILNE EDWARDS, H., and LUCAS, H., 1841, Description des Crustace´s nouveaux ou skrift, v. 2, p. 249–261. peu connus conserve´s dans la collection du Muse´um d’Histoire naturelle: Archives LABADIE, L.V., and PALMER, A.R., 1996, Pronounced heterochely in the ghost shrimp, du Muse´um, v. 2, p. 461–483, pl. 24–28. Neotrypaea californiensis (Decapoda: Thalassinidea: Calianassidae): Allometry, MORI, M., 1986, Contributions to the biology of Paromola cuvieri (Crustacea: inferred function and development: Journal of the Zoological Society of London, Decapoda: Homolidae) in the Ligurian Sea: Oebalia, v. 13, p. 49–68. v. 240, p. 659–675. MORI, M., ABELLO´ , P., MURA, M., and DE Ranieri, S., 1995, Population charac- LAMARCK, J.B.P.A. DE, 1818, Histoire Naturelle des Animaux sans Verte`bres, teristics of the crab Monodaeus couchii (Crustacea, Brachyura, Xanthidae) in the pre´sentant les caracte`res ge´ne´raux et particuliers de ces animaux, leur distribution, western Mediterranean: Miscellania Zoologica, v. 18, p. 77–88. leurs classes, leurs familles, leurs genres, et la citation des principales espe`ces qui s’y MU¨ LLER, P., 1984, Decapod Crustacea of the Badenian: Geologica Hungarica, Series rapportent; pre´ce´de´e d’une introduction offrant la de´termination des caracte`res Palaeontologica, v. 42, p. 1–317, pl. 1–97. essentiels de l’Animal, sa distinction du ve´ge´tal et des autres corps naturels, enfin, NG, P.K.L., and TAN, L.W.H., 1984, The ‘Shell Peeling’’ structure of the box crab, l’Exposition des principes fondamentaux de la zoologie, edition 5: De´terville, Paris, Calappa philargius (Linn.) and other crabs in relation to mollusc shell architecture: p. 1–612. Journal of the Singapore National Academy of Science, v. 13, p. 195–199. LATREILLE, P.A., 1802–1803, Histoire naturelle, ge´ne´rale et particulie`re, des crustace´s OJI, T., OGAYA, C., and SATO, T., 2003, Increase in shell-crushing predation recorded et des insectes, Volume 3: F. Dufart, Paris, p. 1–468. in shell fragmentation: Paleobiology, v. 29, p. 520–526. ATREILLE L , P.A., 1817, Nouveau dictionnaire d’histoire naturelle, applique´e aux ORTMANN, A., 1893, Abtheilung: Brachyura (Brachyura genuina Boas), II. arts, a` l’agriculture, a` l’economie rurale et domestique, a`lame´decine, etc., v. 10: Unterabtheilung: Cancroidea, 2. Section: Cancrinea, 1. Gruppe: Cyclometopa. De´terville, Paris, 404 p. Die DecapodenKrebse des Strassburger Museums, mit besonderer Beru¨cksichti- LATREILLE, P.A., 1825, Genre de Crustace´s: Encyclopedie methodique: Histoire gung der von Herrn Dr. Do¨derlein bei Japan und bei den Liu-Kiu-Inseln naturelle: Entomologie, ou histoire naturelle des Crustace´s, des Arachnides et des gesammelten und zur Zeit im Strassburger Museum aufbewahrten Formen, VII. Insectes: Paris, v. 10, p. 1–832. Theil: Zoologische Jahrbu¨cher, Abtheilung fu¨r Systematik, Geographie, und LAU, C. J., 1987, Feeding behavior of the Hawaiian slipper lobster, Scyllarides Biologie der Thiere, v. 7, p. 411–495, pl. 17. squammosus, with a review of decapod crustacean feeding tactics on molluscan PRZIBRAM, H., 1931, Connecting Laws in Animal Morphology: London, University of prey: Bulletin of Marine Science, v. 41, p. 378–391. London Press, p. 13–24. LEACH, W. E., 1814, Crustaceology, in Brewster, D., ed., Edinburgh Encyclopaedia, RACHEBOEUF, P.R., and VILLARROEL, C., 2003, Imocaris colombiensis n. sp. (Crustacea: Volume 7: Balfour, Edinburgh, p. 383–437, pl. 221. Decapoda) from the Pennsylvanian of Colombia: Neues Jahrbuch fu¨r Geologie LEE, S.Y., 1995, Cheliped size and structure: The evolution of a multi-functional und Pala¨ontologie, Monatshefte, v. 10, p. 577–590. decapod organ: Journal of Experimental Marine Biology and Ecology, v. 193,p. RAFINESQUE, C.S., 1815, Analyse de la Nature, ou Tableau de l’Univers et des corps 161–176. organise´e: L’Imprimerie de Jean Barravecchia, Palermo, Italy, 224 p. LINNAEUS,C.VON, 1758, Systema naturae per regna tria naturae, secundum classes, RANDALL, J.W., 1840, Catalogue of the Crustacea Brought by Thomas Nuttall and J. ordines, genera, species, cum characteribus, differentiis, synonymis, locis: Edition K. Townsend, from the West Coast of North America and the Sandwich Islands, 10, volume 1, Laurentii Salvii Homiae (5 Stockholm), 824 p. with Descriptions of Such Species As Are Apparently New, among Which Are LINNAEUS,C.VON, 1767, Systema Naturae per Regna tria Naturae, secundum classes, Included Species of Different Localities, Previously Existing in the Collection of the ordines, genera, species, cum characteribus, differentiis, synonymis, locis: (edit. 12) Academy. Journal of the Academy of Natural Sciences of Philadelphia: v, 8, p. 1(2), p. 533–1327. 106–147. LOVRICH, G.A., and SAINTE-MARIE, D., 1997, Cannibalism in the snow crab RATHBUN, M.J., 1896, The genus Callinectes: Proceedings of the United States Chionoecetes opilio (O. Fabricius) (Brachyura: Majidae), and its potential National Museum, v. 18, p. 349–375, pl. 12–28. importance to recruitment: Journal of Experimental Marine Biology and Ecology, RATHBUN, M.J., 1904, Some changes in Crustacean nomenclature: Proceedings of the v. 211, p. 225–245. Biological Society of Washington, v. 17, p. 169–172. PALAIOS DECAPODA AS PREDATORS ON MOLLUSCA OVER GEOLOGIC TIME 181

RATHBUN, M.J., 1916, Description of a new genus and species of fossil crab from Port SCHWEITZER, C.E., and FELDMANN, R.M., 2000a, New species of calappid crabs from Townsend, Washington: American Journal of Science, v. 41, p. 344–346. Western North America and reconsideration of the Calappidae de Haan sensu lato: RATHBUN, M.J., 1917, New species of South Dakota Cretaceous crabs: Contributions Journal of Paleontology, v. 74, p. 230–246. to Zoology, v. 67, p. 237–255. SCHWEITZER, C.E., and FELDMANN, R.M., 2000b, Reevaluation of the Cancridea RATHBUN, M.J., 1923, Decapod crustaceans from the Upper Cretaceous of North Latreille, 1803 (Decapoda: Brachyura) including three new genera and three new Carolina: North Carolina Geological Survey, v. 5, p. 403–407. species: Contributions to Zoology, v. 69, p. 233–250. RATHBUN, M.J., 1926, The fossil stalk-eyed Crustacea of the Pacific Slope of North SCHWEITZER, C.E., and FELDMANN, R.M., 2001, New Cretaceous and Tertiary America: United States National Museum, Bulletin 138, viii + 155 p. decapod crustaceans from western North America. Bulletin of the Mizunami Fossil RATHBUN, M.J., 1935, Fossil Crustacea of the Atlantic and Gulf Coastal Plain: Museum, v. 28, p. 173–210. Geological Society of America Special Paper, v. 2, p. viii + 1–160. SCHWEITZER, C.E., and FELDMANN, R.M., 2005, Decapods, the Cretaceous-Palaeogene REUSS, A.E., 1859, Zur Kenntnis fossiler Krabben: Akademie der Wissenschaften Boundary, and Recovery, in Koenemann, S. and Jenner, R.A., eds., Crustacea and Wien, Denkschrift, v. 17, p. 1–90, pl. 1–24. Arthropod Relationships,Crustacean Issues V. 16: Taylor and Francis Group, RICHARDS, B.C., 1975, Longusorbis cuniculosis: a new genus and species of Upper Boca Raton, p. 17–53. Cretaceous crab; with comments on Spray Formation at Shelter Point, Vancouver SCHWEITZER, C.E., and FELDMANN, R.M., 2009, Revision of the Prosopinae sensu Island, British Columbia: Canadian Journal of Earth Sciences, v. 12, p. 1850–1863. Glaessner, 1969 (Crustacea: Decapoda: Brachyura) including 4 New Families and 4 RINEHART, L.F., LUCAS, S.G., and HECKERT, A.B., 2003, An early eubrachyuran New Genera: Annalen des Naturhistorischen Museums in Wien, Serie A, v. 110,p. (Malacostraca: Decapoda) from the Upper Triassic Snyder Quarry, Petrified 55–121. Forest Formation, north-central New Mexico, in Zeigler, K.E., Heckert, A.M., and SCHWEITZER, C.E., FELDMANN, R.M., and KARASAWA, H., 2007, Revision of the Lucas, S.G., eds., Paleontology and Geology of the Upper Triassic (Revueltian) Carcineretidae Beurlen, 1930 (Decapoda: Brachyura: Portunoidea) and remarks on Snyder Quarry, New Mexico: New Mexico Museum of Natural History & Science the Portunidae Rafinesque, 1815: Annals of Carnegie Museum, v. 76, p. 15–37. Bulletin 24, p. 67–70. SCHWEITZER, C.E., FELDMANN, R.M., GONZA´ LEZ-BARBA, G., and C´ OSOVIC´ , V., 2006, ROBLES, C., SWEETNAM, D., and EMINIKE, J., 1990, Lobster predation on mussels: New Decapoda (Anomura, Brachyura) from the Eocene Bateque and Tepetate Shore-level differences in prey vulnerability and predator preference: Ecology, v. Formations, Baja California Sur, Mexico: Bulletin of the Mizunami Fossil 71, p. 1564–1577. Museum, v. 33, p. 21–45. OCHETTE OYLE DGELL R , R., D , S.P. and E , T.C., 2007, Interaction between an invasive SCHWEITZER, C.E., FELDMANN, R.M., GONZA´ LES-BARBA, G., and VEGA, F.J., 2002, decapod and native gastropod: Predator foraging tactics and prey architectural New crabs from the Eocene and Oligocene of Baja California Sur, Mexico and an defenses: Marine Ecology Progress Series, v. 330, p. 179–188. assessment of the evolutionary and paleobiogeographic implications of Mexican ROMERO, M.C., LOVRICH, G.A., TAPELLA, F., and THATJE, S., 2004, Feeding ecology of fossil decapods: Paleontological Society Memoir 76, 43 p. the crab Munida subrugosa (Decapoda: Anomura: Galatheidae) in the Beagle SCHWEITZER, C.E., FELDMANN, R.M., GARASSINO, A., KARASAWA, H., and SCHWEIGERT, Channel, Argentina: Journal of the Marine Biological Association of the United G., 2010, Systematic list of fossil decapod crustacean species: Crustacean Kingdom, v. 84, p. 359–365. Monographs, v. 10, 230 p. RORANDELLI, R., GOMEI, M., VANNINI, M., and CANNICCI, S., 2007, Feeding and SCHWEITZER, C.E., FELDMANN, R.M., & KARASAWA, H., 2007, Revision of the masking selection in Inachus phalangium (Decapoda, Majidae): Dressing up has Carcineretidae Beurlen, 1930 (Decapoda: Brachyura: Portunoidea) and remarks on never been so complicated: Marine Ecology Progress Series, v. 336, p. 225–233. the Portunidae Rafinesque, 1815: Annals of Carnegie Museum, v. 76, no. 1, p. 15– SAMOUELLE, G., 1819, The entomologist’s useful compendium, or an introduction to 37. the British insects, etc.: T. Boys, London, 496 p. SCHWEITZER, C.E., ARTAL, P., VAN BAKEL, B., JAGT, J.W.M., and KARASAWA, H., 2007, SAMSON, S.A., YOKOTA, M., STRU¨ SSMANN, C.A., and WATANABE, S., 2007, Natural diet Revision of the genus Titanocarcinus (Decapoda: Brachyura: Xanthoidea) with two of grapsoid crab Plagusia dentipes de Haan (Decapoda: Brachyura: Plagusiidae) in new genera and one new species: Journal of Crustacean Biology, v. 27, p. 278–295. Tateyama Bay, Japan: Fisheries Science, v. 73, p. 171–177. SEED, R., 1993, Crabs as predators of marine bivalve molluscs, in Morton, B., eds., SANTOS, S., AYRES-PERES, L., CARDOSO, R.C.F., and SOKOLOWICZ, C.C., 2008, Natural The Marine Biology of the South China Sea: Proceedings of the First International diet of the freshwater anomuran Aegla longirostri (Crustacea, Anomura, Aeglidae): Conference on the Marine Biology of Hong Kong and the South China Sea, Hong Journal of Natural History, v. 42, p. 1027–1037. Kong, 28 October–3 November 1990: Hong Kong University Press, Hong Kong, p. SASAKI, J., and KUWAHARA, Y., 1999, Stomach contents of the Hanasaki crab, 393–418. Paralithodes brevipes (Lithodidae, Anomura, Decapoda) sampled from the littoral SEED, R., and HUGHES, R.N., 1995, Criteria for prey size-selection in molluscivorous zone off Nemuro Peninsula: Scientific Report of the Hokkaido Fisheries crabs with contrasting claw morphologies: Journal of Experimental Marine Experimental Station, v. 55, p. 169–172. Biology and Ecology, v. 193, p. 177–195. SCHEMBRI, P.J., 1982, Feeding behaviour of fifteen species of hermit crabs (Crustacea: Decapoda: Annomura) from the Otago region, southeastern New Zealand: Journal SHOUP, J. B., 1968, Shell opening by crabs of the genus Calappa: Science, v. 160, p. of Natural History, v. 16, p. 859–878. 887–888. SIMONSON, J. L., 1985, Reversal of handedness, growth, and claw stridulatory patterns SCHENK, S.C., and WAINWRIGHT, P.C., 2001, Dimorphism and the functional basis of claw strength in six brachyuran crabs: Journal of Zoology, London, v. 255, p.105– in the stone crab Menippe mercenaria (Say) (Crustacea: Xanthidae): Journal of 119. Crustacean Biology, v. 5, p. 281–293. SMITH, L.D., and PALMER, A.R., 1994, Effects of manipulated diet on size and SCHRAM, F.R., 1980, Miscellaneous late Paleozoic Malacostraca of the Soviet Union: Journal of Paleontology, v. 54, p. 542–547. performance of brachyuran crab claws: Science, v. 264, p. 710–712. SCHRAM, F.R.,1986, Crustacea: Oxford University Press, New York, 606 p. SQUIRES, H.J., and DAWE, E.G., 2003, Stomach contents of snow crab (Chionoecetes SCHRAM, F.R., and MAPES, R.H., 1984, Imocaris tuberculata, n. gen., n. sp. opilio, Decapoda, Brachyura) from the northeast Newfoundland Shelf: Journal of (Crustacea: Decapoda) from the upper Mississippian Imo Formation, Arkansas: Northwest Atlantic Fisheries Science, v. 32, p. 27–38. Transactions of the San Diego Society of Natural History, v. 20, p. 165–168. STANLEY, S. M., 2008, Predation defeats competition on the seafloor: Paleobiology, v. SCHRAM, F.R., FELDMANN, R.M., and COPELAND, M.J., 1978, The late Devonian 34, p. 1–21. Palaeopalaemonidae and the earliest decapod crustaceans: Journal of Paleontol- STENZEL, H.B, 1945, Decapod crustaceans from the Cretaceous of Texas: The ogy, v. 52, p. 1375–1387. University of Texas Publication, v. 4401, p. 401–477. SCHWEITZER, C.E., 2000. Tertiary Xanthoidea (Decapoda: Brachyura) from the Pacific STEPHENSON, W., and CAMPBELL, B., 1960, The Australian portunids (Crustacea: Northwest of North America: Journal of Crustacean Biology, v. 20, p. 715–742. Portunida) IV: Remaining genera: Australian Journal of Marine and Freshwater SCHWEITZER, C.E., 2001a, Additions to the Tertiary decapod fauna of the Pacific Research, v. 11(1), p. 73–122, pl. 1–6. Northwest of North America: Journal of Crustacean Biology, 21, p. 521–537. STIMPSON, W., 1866, Descriptions of new genera and species of Macrurous Crustacea SCHWEITZER, C.E., 2001b, Paleobiogeography of Cretaceous and Tertiary decapod from the coasts of North America: Proceedings of the Chicago Academy of crustaceans of the North Pacific Ocean: Journal of Paleontology, v. 75, p. 808–826. Sciences, v. 1, p. 46–48. SCHWEITZER, C.E., 2003, Utility of proxy characters for classification of fossils: An SUKUMARAN, K.K., and NEELAKANTAN, B., 1997, Food and feeding of Portunus example from the fossil Xanthoidea (Crustacea: Decapoda: Brachyura): Journal of (Portunus) saunguinolentus (Herbst) and Portunus (Portunus) pelagicus (Linnaeus) Paleontology, v. 77, p. 1107–1128. (Brachyura: Portunidae) along Karnataka coast: Indian Journal of Marine SCHWEITZER, C.E., 2005a, The genus Xanthilites Bell, 1858 and a new xanthoid family Sciences, v. 26, p. 35–38. (Crustacea: Decapoda: Brachyura: Xanthoidea): New hypotheses on the origin of TAYLOR, G.M., 2001, The evolution of armament strength: Evidence for a constraint the Xanthoidea MacLeay, 1838: Journal of Paleontology, v. 79, p. 277–295. on the biting performance of claws of durophagous decapods: Evolution, v. 55, p. SCHWEITZER, C.E., 2005b, The Trapeziidae and Domeciidae (Decapoda: Brachyura: 550–560. Xanthoidea) in the fossil record and a new Eocene genus from Baja California Sur, THOMAS, H.J., and DAVIDSON, C., 1962, The food of the Norway lobster Nephrops Mexico: Journal of Crustacean Biology, v. 25, no. 4, p. 625–636. norvegicus (L.): Marine Research, v. 3, p. 1–15. 182 SCHWEITZER AND FELDMANN PALAIOS

VAN STRAELEN, V., 1924 [imprint 1925], Contribution a` l’e´tude des crustace´s WAUGH, D.A., FELDMANN, R.M., SCHROEDER, A.M., and MUTEL, M.H.E., 2006, de´capodes de la pe´riode jurassique: Memoires d’Academie Royale de Belgique, Differential cuticle architecture and its preservation in fossil and extant Callinectes Cl. Sci., collected in number 4, series 2, v. 7, p. 1–462, pl. 1–10. and Scylla claws: Journal of Crustacean Biology, v. 26, p. 271–282. VANNINI,M.,CHELAZZI,G.,andCHERARDI, F., 1989, Feeding habits of the pebble crab WELLER, S., 1903, The Stokes collection of Antarctic fossils: Journal of Geology,v. Eriphia smithi (Crustacea, Brachyura, Menippidae): Marine Biology, v. 100, p. 249–252. 11, p. 413–419. VEGA, F.J., FELDMANN, R.M., GARCı´A-BARRERA, P., FILKORN, H., PIMENTEL, F., and WHITE, A., 1847, List of the specimens of Crustacea in the collection of the British AVENDAN˜ O, J., 2001, Maastrichtian Crustacea (Brachyura: Decapoda) from the Museum: British Museum, London, 143 p. Ocozocuautla Formation in Chiapas, Southeast Mexico: Journal of Paleontology, WHITFIELD, R.P., 1880, Notice of new forms of fossil crustaceans from the upper v. 75, p. 319–329. Devonian rocks of Ohio, with description of new genera and species: American VEGA, F. J., FELDMANN, R.M., OCAMPO, A.O., & POPE, K.O., 1997, A new species of Journal of Science, Series 3, v. 19, p. 33–42. Late Cretaceous crab (Brachyura: Carcineretidae) from Albion Island, Belize: WHITFIELD, R.P., 1907, Notice of an American species of the genus Hoploparia Journal of Paleontology, v. 71, no. 4, p. 615–620. McCoy, from the Cretaceous of Montana: American Museum of Natural History VERMEIJ, G.J., 1977a, The Mesozoic marine revolution: evidence from snails: Bulletin, v. 23, p. 459–461. Predators and grazers: Paleobiology, v. 3, p. 245–258. WILLIAMS, M.J., 1978, Opening of bivalve shells by the mud crab Scylla serrata VERMEIJ, G.J., 1977b, Patterns in crab claw size: The geography of crushing: Forska˚l: Australian Journal of Marine and Freshwater Research, v. 29, p. 699–702. Systematic Zoology, v. 26, p. 138–151. WINKLER, T.-C., 1883, E´ tude carcinologique sur les genres ‘‘Pemphix,’’ ‘‘Glyphea’’ et VERMEIJ, G.J., 1987, Evolution and Escalation: Princeton University Press, Princeton, ‘‘Araeosternus:’’ Archives du Muse´e Teyler, v. 2, no. 1, p. 73–124. 527 p. WITHERS, T.H., 1922, On a new brachyurous crustacean from the Upper VERMEIJ, G.J., 2002, Evolution in the consumer age: Predators and the history of life, Cretaceous of Jamaica, Annals and Magazine of Natural History, 9th series, in Kowalewski, M., and Kelley, P.H., eds., The Fossil Record of Predation: v. 10, p. 534–541. Paleontological Society Papers 8, p. 375–393. WOOD-MASON, J., and ALCOCK, A., 1891, A note on the result of the last season’s VERMEIJ, G.J., 2008, Escalation and its role in Jurassic biotic history: Palaeogeo- graphy, Palaeoclimatology, Palaeoecology, v. 263, p. 3–8. deep-sea dredging: natural history notes from H. M. Indian Marine Survey Steamer ‘‘Investigator’’: Commander R. F. Hoskyn, R. N. Commanding, no. 21: VI´A, L., 1959, Deca´podos fo´siles del Eoceno espanol: Boletin del Instituto Geolo´gico y Minero de Espana, v. 70, p. 1–72. Annals and Magazine of Natural History, 6, v. 7, p. 258–272. OODS VON MEYER, H., 1840, Briefliche Mitteilungen: Neues Jahrbuch fu¨r Mineralogie, W , H., 1925–1931, A Monograph of the Fossil Macrurous Crustacea of Geologie, Geognosie und Petrefaktenkunde, v. 1840, p. 587. England: Palaeontographical Society, London, 122 p. WALKER, S.E., and BRETT, C.E., 2002, Post-Paleozoic patterns in marine predation: WOODS, C.M.C., 1993, Natural diet of the crab Notomithrax ursus (Brachyura: Was there a Mesozoic and Cenozoic marine predatory revolution?, in Kowalewski, Majidae) at Oaro, South Island, New Zealand: New Zealand Journal of Marine M., and Kelley, P.H., eds., The Fossil Record of Predation: The Paleontological and Freshwater Research, v. 27, p. 309–315. Society Papers, vol. 8: The Paleontological Society, p. 119–193. YAMADA, S.B., and BOULDING, E.G., 1998, Claw morphology, prey size selection and WARNER, G.F., 1977, The Biology of Crabs: Van Nostrand Reinhold Company, New foraging efficiency in generalist and specialist shell-breaking crabs: Journal of York, 202 p. Experimental Marine Biology and Ecology, v. 220, p. 191–211. WARNER, G.F., and JONES, A.R., 1976, Leverage and muscle type in crab chelae ZIPSER, E., and VERMEIJ, G.J., 1978, Crushing behavior of tropical and temperate (Crustacea: Brachyura): Journal of the Zoological Society of London, v. 180, p. 57–68. crabs: Journal of Experimental Marine Biology and Ecology, v. 31, p. 155–172. WASSENBERG, T.J., and HILL, B.J., 1989, Diets of four decapod crustaceans (Linuparus trigonus, Metanephrops andamanicus, M. australiensis, and M. boschmai) from the continental shelf around Australia: Marine Biology, v. 103, p. 161–167. ACCEPTED NOVEMBER 24, 2009